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Diet of the Barn Owl (Tyto alba Scopoli 1769) from the Copiapo Valley, Atacama Desert, Chile/Dieta de la lechuza blanca (Tyto alba scopoli 1769) en el Valle De Copiapo, Desierto De Atacama, Chile/Dieta da coruja-das-torres (Tyto alba scopoli 1769) no Vale De Copiapo, Deserto De Atacama, Chile.

Introduction

The nocturnal raptor Tyto alba (Scopoli, 1769) is a member of the Strigidae family, a raptor species which is one of the most widespread of all birds in the world (Clark et al, 1978). In Chile, this raptor is found across the entire country, inhabiting a large diversity of environments (Carmona and Rivadeneira, 2006).

There are many dietary studies of the Barn Owl in South America, for example in Argentina (Noriega, 1993, Solaro, 2012; Gomez, 2012; Bellocq and Kravetz, 1994; Donadio, 2009; Nanni et al., 2012; Sahores and Trejo, 2004; Fernandez et al., 2009; Travaini et al., 1997), Bolivia (Vargas et al., 2002; Reboledo and Lartigau, 1998; Aliaga-Rossel and Tarifa, 2005), Brazil (Bonvicino and Bezerra, 2003; Rocha et al., 2011; Moura de Faria and Passamani, 2013), Colombia (Delgado and Ramirez, 2007, 2009), Cuba (Lopez Ricardo, 2012; Hernandez-Munoz and Mancina, 2011), Peru (Ramirez et al., 2000) and Venezuela (Araujo and Molinari, 2000). In the rest of the world, many others studies have been published, for example in Australia (Debus et al., 2004), France (Bernard et al., 2010), India (Patki et al., 2014), Italy (Catalisano and Massa, 1987; Pezzo and Morimando, 1995), Netherlands (De Bruijn, 1994), Pakistan (Khan et al., 2014), Poland (Kitowski, 2013; Kopij, 2012), Spain (Brana, 1974; Herrera, 1973; Sans-Coma, 1974; Siverio et al., 2010; Zamorano et al., 1986; Sommer et al., 2005), Syria (Shehab and Al Sharabi, 2006) and USA (Michel, 2009; Colvin and McLean, 1986; Marti, 2010).

In Chile, the dietary habits of the Barn Owl are considered the best known among all the raptors inhabiting the territory (Raimilla et al., 2012) although many other biological variables remain poorly understood or unknown.

In general, the diet of the Chilean population of Barn Owl is composed mainly of small mammals, particularly nocturnal rodents (Jaksic and Yanez, 1979; Cerpa and Yanez, 1981, Jaksic et al., 1981), although other important items are marsupials, birds and arthropods. The diet of this raptor has been studied in many Chilean locations, such as Chiu-Chiu, Antofagasta region (Jaksic et al., 1999), La Dehesa, Metropolitana region (Reise, 1970); Fray Jorge, Coquimbo region (Schamberger and Fulk, 1974); Puchuncavi (Cerda and Yanez, 1981) and La Campana (Zunino and Arcos, 1989) both in Valparaiso region; Lastarria, Araucania region (Rau et al., 1985); Termas del Flaco, Libertador Bernardo O'Higgins region (TorresMura and Contreras, 1989); Burca, Concepcion region (Munoz and Murua, 1990); Torres del Paine, Magallanes region (Iriarte et al., 1990); and Pampa del Tamarugal, Tarapaca region (Carmona and Rivadeneira, 2006). The diet of the Barn Owl has been studied in almost all regions of Chile, the Atacama region being an exception. For this reason, the aim of the present study is to analyze the diet of the Barn Owl from the Atacama region, specifically in the Copiapo valley. This valley is located in close ecological relationship to a hyper-arid area, where sporadic rainfall triggers the blossoming of a large diversity of endemic plants and flowers. This phenomenon is known as 'flowering desert' and the areas where it occurs are considered a Priority Conservation Site Desierto Florido (Squeo et al., 2008).

Methods

The study was conducted in the Copiapo valley (35[degrees]15'47"S, 69[degrees]78'10"W, 221masl), in the Atacama Desert, Northern Chile. The ecological conditions of the Atacama Desert region correspond to a hyper-arid area (Julia et al., 2008) known as 'flowering desert of the plains' (Gajardo, 1994), with a transitional desert climate (Novoa et al., 2008; Julia et al., 2008) and geo-morphologically named transitional Pampa (Novoa et al., 2008). In terms of eco-geographical landscape, the study area includes two areas denominated Pampa and Serrano, with the lowest rainfall in the region (<0.5mm in normal conditions).

Pellets were collected under the higher trees, particularly palms from the localities of Piedra Colgada (n= 107) and San Pedro (n= 42) in MayOctober 2011 and JuneDecember 2012, near Copiapo city, Atacama region. Both localities correspond to a transversal valley with agricultural systems. Collected pellets were stored in paper bags with a label indicating date of collection, a unique numeric code and the number of pellets found in the particular location. The pellets were transported to the Laboratory of Integrative Zoology, Universidad de Tarapaca, Arica, Chile. The pellets were individually hydrated for 3h. Subsequently, the pellets were disaggregated and all remains were identified to the highest possible taxonomic level. The analysis of bones (skulls and jaws) and exoskeleton fragments was performed under a stereomicroscope (Olympus XTL-2310). For the recognition of the prey species, we used skull and jaw as reference keys for rodents and lizards that inhabit the Atacama region. These references are in the Zoological Collection of Arid and Andean Zones, Universidad de Tarapaca (CZZAUTA). Identification of arthropods was achieved by applying the methodology described by Cepeda-Pizarro et al. (2005).

Each identified prey item was recorded in a database, and frequency and abundance in each pellet were calculated. The number of vertebrate individuals in each pellet was determined using either skulls or maximum count of jaws. On the other hand, the number of insect preys was established using heads or pairs of elytra. To analyze the contribution of each prey in biomass consumption the number of individuals in each pellet was multiplied by the average mass (g) of each species. This mass value was obtained from previous studies carried out by Cortes et al. (1992) for lizards, Spotorno et al. (1998) for Oligoryzomys, Abrothrix and Abrocoma, Spotorno et al. (2013) for Eligmodontia and by Cepeda-Pizarro et al. (2005) for arthropods. Subsequently, in order to assess dietary preference for body size or habitat preference of the prey, a linear Pearson correlation analysis was performed between the frequencies for prey and body mass, and between number of prey and type of habitat. Finally Simpson and Shannon indices were calculated to assess the richness of preys (Munoz-Pedreros and Rau, 2004). Statistical analyzes were performed using SPSS 10.0 software.

Results

One hundred forty nine pellets were analyzed, resulting in a total of 275 prey items identified (Table I). The group mostly consumed was rodents, with an abundance of 76.7%. Of these, the largest prey item (27.3%) corresponds to species of small animals such as Eligmodontia dunaris (Spotorno et al., 2013), and other median and large rodents such as Phyllotis darwini (Waterhouse, 1837) (24%) and Abrocoma bennetti Waterhouse, 1837 (12.4%). Other species were birds (17.8%), including Zonotrichia capensis (Muller, 1776) (2.9%), Troglodytes aedon Vieillot, 1809 (3.3%) and Diuca diuca (Molina, 1782) (3.3%). Occasional items found were coleopterans (3.3%) and lizards from the Liolaemus genus (0.4%).

The group that contributes most to the total biomass is that of mammals (96.4%), particularly A. bennetti (60.1%), and secondarily P. darwini (26.8%) and E. dunaris (6.3%). Contributions of others species were not significant, for example birds (3.5%), coleopterans (0.1%) and lizards (0.1%) (Table II). There was no significant correlation between frequency of prey and their body mass ([r.sup.2] = 0.229, p = 0.497) and between frequency and their habitat ([r.sup.2] = 0.538, p = 0.088), both indicating that this raptor does not select their prey by body size or habitat. Finally, both the Simpson index (SI = 0.1683) and the Shannon index (H' = 0.8958) indicate a low diversity of prey, which is consistent with the others raptors that inhabit on arid environments.

Discussion

Our work corresponds to first record of the diet of the Barn Owl from the Atacama region, Chile. The diet of this raptor in the Atacama Desert is primarily composed of smaller mammals of the genus Eligmodontia, followed by Phyllotys darwini and Abrocoma bennetti. These data are in agreement with those found in the literature, where the preference is mammals, values ranging from 76.2% in Tamarugal, northern Chile, to 99.8% in the Torres del Paine, Southern Chile (Carmona and Rivadeneira, 2006). In other studies similar results are found in the consumption of birds: 3.4% in Tamarugal and 0.2% in Torres del Paine (range 0.2-10%), those of reptiles and amphibians are not significant, and arthropods are more important than in the present our study (range 2-16.4%). The smaller marsupial Thylamys elegans (Waterhouse, 1839) was less consumed in Atacama than T. pallidior (Thomas, 1902) in Tamarugal (range 6.7-25.9%).

On the other hand, A. bennetti and Oligoryzomys longicaudatus (Bennett, 1832) inhabit the valleys of the Atacama region (Valladares and Campo, 2012) with vegetation cover, scrub and farm fields. P. darwini lives in arid hills and ravines (Valladares, 2012) and E. dunaris is a small rodent which inhabits in the arid dunes under small scrubs, where they dig their burrows (Spotorno et al., 2013). Despite the fact that the Barn Owl build their nests in the valley of Copiapo, their prey is principally captured from desert and ravines (53.1%), whereas prey from the valleys constitute only 16%. Especially interesting is the complete absence of Rattus sp. in the diet of the Barn Owl from the Copiapo valley, despite the abundance of this species in these areas and in the city. The differences in the proportions of mammals and birds consumed may be related to the coincidence in daily activity, since most species of rodents have crepuscular or nocturnal rather than diurnal activities (Iriarte, 2008).

The Shannon and Simpson indices indicate a low diversity of prey in the population of T. alba from the Atacama region, compared with populations of southern Chile and Argentina, where the number of prey increases to more than double. Considering indirect variables such as the wider distribution range and its fundamental trophic niche, displayed on the large number of prey registered, it could be indicating an ecologically generalist species (Futuyma and Moreno, 1988; Kassen, 2002; Calenge and Basille, 2008), and these results indicate a functional response to prey availability (Jaksic et al., 1992; Farias and Jaksic, 2007).

This study is of relevance since the population of Barn Owl inhabit the Priority Conservation Site Desierto Florido (Squeo et al., 2008). When the El Nino phenomenon (ENSO) takes place, rainfall increases and the area blooms, with subsequent changes in populations of all the species that live there. The present data were obtained when rainfall was very low. Therefore this work constitutes a first diagnosis of the dietary biology of the Barn Owl in the Atacama region, which must be also assessed when an ENSO phenomenon occurs, allowing a clearer idea of the consequences of this phenomenon on the biological communities of the Atacama Desert.

Received: 06/02/2015. Modified: 01/21/2016. Accepted: 01/21/2016.

Pablo Valladares Faundez.

Biologist, Universidad Austral de Chile. Doctor in Biomedical Sciences, Universidad de Chile. Professor, Universidad de Tarapaca, Chile. Address: Departamento de Biologia, Facultad de Ciencias, Universidad de Tarapaca. Avenida General Velasquez 1775, Arica, Chile. e-mail: pvalladares@uta.cl

Natalia Urrutia Osorio. Graduate in Education and as Teacher of Biology and Natural Sciences, Universidad de Tarapaca, Chile. Professor, Universidad La Republica, Arica, Chile.

Nicole Alvarez Henriquez. Graduate in Education and as Teacher of Biology and Natural Sciences, Universidad de Tarapaca, Chile. Professor, Universidad La Republica, Arica, Chile.

Osman Orellana Orozco. Graduate in Education and as Teacher of Biology and Natural Sciences, Universidad de Tarapaca, Chile.

Sergio Alvarado Orellana. M.Sc. in Biostatistics and M.Sc. en Ecologia y Biologia Evolutiva, Universidad de Chile. Ph.D., Universidad Autonoma de Barcelona, Spain. Professor, Universidad de Chile.

ACKNOWLEDGEMENTS

The authors thank Wladimir Wilkomirsky for allowing the collection of pellets of T. alba at his property in the locality of Piedra Colgada, the University of Tarapaca for Project No. 4710-15, Paola Moraga for help in processing the pellets and Patricio Velez for help in translation.

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TABLE I
BARN OWL (Tyto alba) PREY RECORDED IN
COPIAPO VALLEY, ATACAMA REGION

Item prey                  Abundance     Frequency

Rodentia                    N      %     Nf    %

  Abrothrix olivaceus       4     1.5    4    2.7
  Phyllotis darwini        66    24.0    45   30.2
  Oligorysomys              6     2.2    6    4.0
    longicaudatus
  Eligmodontia dunaris     75    27.3    43   28.9
  Abrocoma bennetti        34    12.4    32   21.5
  Non identified rodents   26     9.5    26   17.4
                                 76.7
Didelphimorphia
  Thylamys elegans          5     1.8    4    2.7

Passeriformes
  Zonotrichia capensis      8     2.9    8    5.4
  Troglodytes aedon         9     3.3    9    6.0
  Diuca diuca               9     3.3    8    5.4
  Non identified birds     23     8.4    22   14.8
                                 17.8
Coleoptera
  Gyriosomus sp.            9     3.3    9    6.0
Squamata
  Liolaemus sp.             1     0.4    1    0.7
Total                      275   194.5

TABLE II
BIOMASS PROVIDED BY EACH PREY
ITEMS IN THE DIET OF BARN OWL *

                               No. of   Mass/sp    Total       %
                               items     (gr)     biomass   Biomass
                                                   (gr)

Mammalia
  Abrothrix olivaceus            4        35        140       0.5
  Phyllotis darwini              66      57.5      3795      26.8
  Oligorysomys longicaudatus     6       27.8      166.8      1.2
  Eligmodontia dunaris           75      11.9      892.5      6.3
  Abrocoma bennetti              34      250.5     8517      60.1
  Non identified rodents         26
                                                  13511.3    95.3
Didelphimorphia
  Thylamys elegans               5        30        150       1.1
  Passeriformes
  Zonotrichia capensis           8       22.7      181.6      1.3
  Troglodytes aedon              9       11.3      101.7      0.7
  Diuca diuca                    9       24.2      217.8      1.5
  Non identified birds           23
                                                   501.1      3.5
Coleoptera
  Gyriosomus sp.                 9        0.8       7.2       0.1
Squamata
  Liolaemus sp.                  1       13.3      13.3       0.1

* Average body mass by species collected from Mann (1978),
Cofre and Marquet (1999), Munoz-Pedreros and Yanez (2009)
and Iriarte (2008) for mammals; Anderson et al., (2002)
and Salvador and Bodrati (2013) from birds. Reptiles and
arthropods own data.
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Title Annotation:texto en ingles
Author:Faundez, Pablo Valladares; Osorio, Natalia Urrutia; Henriquez, Nicole Alvarez; Orozco, Osman Orellan
Publication:Interciencia
Date:Feb 1, 2016
Words:4262
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